AbstractChemical ecology began with the study of plant-insect interactions. In the nineteenth century, biologists began to realize the profound importance of plant chemistry in determining herbivore choice. Given that plants are the primary source of food in terrestrial ecosystems, the role of plant metabolites in herbivore choice and performance translates to a role in structuring ecological communities.
This work describes natural variation in volatile and non-volatile herbivore-induced metabolites in the native tobacco /Nicotiana attenuata/, and experiments to test the defensive functions of some of these metabolites in nature. The variation described includes natural variation among accessions in herbivore-induced signaling cascades and metabolite production, as well as complex metabolic variation in a class of terpenoid specialized metabolites, the 17-hydroxygeranyllinalool
diterpene glycosides (HGL-DTGs), in response to herbivore-induced signaling. I dissect the contribution of herbivore-induced jasmonate signaling to the regulation of different traits, and present evidence from wild plants that jasmonate regulation is a suitable, although not exclusive criterion for identifying candidate anti-herbivore defense metabolites. I furthermore present evidence that some of these metabolites do in fact function as anti-herbivore defenses for /N. attenuata/ plants in their natural habitat. Specifically, I demonstrate that HGL-DTGs effectively reduce damage from native specialist herbivores, and that green leaf volatile emission mediates indirect defense and increases plant reproduction in nature. The determination of metabolite functions under controlled laboratory conditions is essential but can be misleading: although trypsin protease inhibitors (TPIs) have become a classic example of anti-herbivore defense, I show that they provide little or no direct benefit to plants in the field, and may instead function to support indirect defense. A combination of labo